Covariation of genetic and epigenetic divergence in barn swallows

As populations diverge, genetic differences accumulate across the genome. Although genetic differentiation is well documented, evolutionary change in epigenetic modifications is less well understood. Here, we integrate genomic and methylomic data from 168 barn swallows (Hirundo rustica) to examine the relationship between genetic and epigenetic population divergence at the resolution of CpG islands and single CpG sites. Sampling across all six extant subspecies and two hybrid zones, we assess the roles of genetic ancestry and environment in shaping DNA methylation patterns. Genome-wide methylation differentiation (P _ST) closely mirrors genetic differentiation (F _ST), with secondary contributions from geographic and environmental variation. DNA methylation patterns track the genomic landscape of sequence divergence, especially in CpG islands of nonregulatory regions. Across hybrid zones, DNA methylation levels are associated with nearby cis-acting genetic variation and global genomic ancestry. Moreover, CpG sites exhibit linkage disequilibrium with nearby SNPs, extending over several thousand base pairs within a putative inversion. These results suggest that although environmental effects on genome-wide DNA methylation are present, epigenomic patterns are costructured by the evolutionary processes shaping genetic variation.